REVIEW published: 28 June 2016 doi: 10.3389/fmicb.2016.00979

Bifidobacteria and Butyrate-Producing Colon Bacteria: Importance and Strategies for Their Stimulation in the Human Gut Audrey Rivière, Marija Selak, David Lantin, Frédéric Leroy and Luc De Vuyst * Research Group of Industrial Microbiology and Food Biotechnology, Faculty of Sciences and Bioengineering Sciences, Vrije Universiteit Brussel, Brussels, Belgium

Edited by: Marco Ventura, University of Parma, Italy Reviewed by: Sinead Christine Leahy, AgResearch Limited, New Zealand Christian U. Riedel, University of Ulm, Germany *Correspondence: Luc De Vuyst [email protected] Specialty section: This article was submitted to Microbial Symbioses, a section of the journal Frontiers in Microbiology Received: 29 April 2016 Accepted: 07 June 2016 Published: 28 June 2016 Citation: Rivière A, Selak M, Lantin D, Leroy F and De Vuyst L (2016) Bifidobacteria and Butyrate-Producing Colon Bacteria: Importance and Strategies for Their Stimulation in the Human Gut. Front. Microbiol. 7:979. doi: 10.3389/fmicb.2016.00979

With the increasing amount of evidence linking certain disorders of the human body to a disturbed gut microbiota, there is a growing interest for compounds that positively influence its composition and activity through diet. Besides the consumption of probiotics to stimulate favorable bacterial communities in the human gastrointestinal tract, prebiotics such as inulin-type fructans (ITF) and arabinoxylan-oligosaccharides (AXOS) can be consumed to increase the number of bifidobacteria in the colon. Several functions have been attributed to bifidobacteria, encompassing degradation of non-digestible carbohydrates, protection against pathogens, production of vitamin B, antioxidants, and conjugated linoleic acids, and stimulation of the immune system. During life, the numbers of bifidobacteria decrease from up to 90% of the total colon microbiota in vaginally delivered breast-fed infants to 1011 bacteria per mL of luminal content) and metabolically active microbiota (Figure 1; Whitman et al., 1998; The Human Microbiome Project Consortium, 2012). The immense number of genes (>100 times the number of genes of the human genome) encoded by this microbiota, expands the host’s biochemical and metabolic capabilities substantially (Bäckhed et al., 2005; The Human Microbiome Project Consortium, 2012). Examples of supporting functions of the human gut microbiota are the degradation of otherwise non-digestible food compounds; the transformation of toxic compounds; and the production of essential vitamins, important metabolic end-products, and defending bacteriocins (Sommer and Bäckhed, 2013). Microbial metabolic end-products, which account for one third of the metabolites present in the human blood, play an important role in gut homeostasis and have an impact on host metabolism and health (Wikoff et al., 2009; Hood, 2012; Louis et al., 2014; Sharon et al., 2014; Richards et al., 2016). The short-chain fatty acids (SCFAs) acetate, butyrate, and propionate (typically occurring in a 3:1:1 ratio) are quantitatively (total concentration of 50– 150 mM) and metabolically the most important microbial endproducts of the human colon fermentation process (Louis et al., 2014), as they display several physiological effects (Table 1). Changes in the gut microbiota composition have been associated with disturbed gut barrier functions, increased gut permeability, and increased plasma lipopolysaccharide concentrations (i.e., metabolic endotoxemia), which causes lowgrade inflammation that triggers the development of obesity and metabolic syndrome (Cani et al., 2008). Also other disorders, such as inflammatory bowel disease (IBD, encompassing Crohn’s disease and ulcerative colitis), irritable bowel syndrome (IBS), colorectal cancer, and allergies have been linked to changes in the gut microbiota composition (de Vos and de Vos, 2012; Le Chatelier et al., 2013). During the last years, even associations have been made between the gut microbiota composition and behavioral disorders, such as depression, anxiety disorder, regressive autism, and schizophrenia (Collins et al., 2012; Braniste et al., 2014; Dinan et al., 2015). However, whereas increasing numbers of animal studies provide evidence for cause-and-effect relationships between shifts in gut microbiota composition and certain disorders (as in the case of obesity; Ridaura et al., 2013), it has not been proven yet for humans whether changes in the gut microbiota composition can cause disorders or that these changes are a consequence of the disorders themselves (de Vos and de Vos, 2012). In recent years, a few distinct members of the human gut microbiota have received particular attention because of their dedicated metabolism and central role in gut homeostasis and because their loss adversely affects the remaining

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BIFIDOBACTERIA AND BUTYRATE-PRODUCING COLON BACTERIA Bifidobacterium Species General Aspects Bifidobacteria are Gram-positive, anaerobic, saccharolytic bacteria that belong to the phylum Actinobacteria; they mainly occur in the gastrointestinal tract of mammals, birds, and insects, but are present in sewage, human breast milk, fermented milk, cheeses, and water kefir too (Bottacini et al., 2014; KhodayarPardo et al., 2014; Laureys and De Vuyst, 2014; Laureys et al., 2016). A typical bifidobacterial genome has an average size ranging from 2.0 to 2.8 Mb and is characterized by a high guanine-plus-cytosine content, with numerous genes involved in the uptake and breakdown of carbohydrates from both diet and host origin (Ventura et al., 2014). Bifidobacteria are among the first bacteria to colonize the human gastrointestinal tract and reach their highest proportion in the colon (up to 90% of the total colon microbiota in vaginally delivered breast-fed infants) during the first 12 months of life (Tannock, 2010; Turroni et al., 2012). This abundance significantly decreases over time to

Bifidobacteria and Butyrate-Producing Colon Bacteria: Importance and Strategies for Their Stimulation in the Human Gut.

With the increasing amount of evidence linking certain disorders of the human body to a disturbed gut microbiota, there is a growing interest for comp...
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